Abstract
Transcription factor IID (TFIID) is a cornerstone in the transcription initiation in eukaryotes. It is composed of TBP and approximately 14 different subunits named TBP-associated factors (TAFs). TFIID has a key role in transcription of many genes involved in cell proliferation, cell growth, cell cycle, cell cycle checkpoint, and various other processes as well. Entamoeba histolytica, the protozoan parasite responsible for human amoebiasis, represents a major global health concern. Our research group has previously reported the genes coding the TATA box-binding protein (EhTBP) and TBP-related factor 1 (EhTRF1), which displayed different mRNA levels in trophozoites under different stress conditions. In this work, we identified the TBP-associated factor 1 (Ehtaf1) gene in the E. histolytica genome, which possess a well-conserved DUF domain and a Bromo domain located in the middle and C-terminus of the protein, respectively. The EhTAF1-DUF domain tertiary structure is similar to the corresponding HsTAF1 DUF domain. RT-qPCR experiments with RNA isolated from trophozoites harvested at different time points of the growth curve and under different stress conditions revealed that the Ehtaf1 gene was found slightly upregulated in the death phase of growth curve, but under heat shock stress, it was found upregulated 10 times, suggesting that Ehtaf1 might have an important role in the heat shock stress response. We also found that EhTAF1 is expressed in the nucleus and cytoplasm at 37 °C, but under heat shock stress, it is overexpressed in both the nucleus and cytoplasm, and partially colocalized with EhHSP70 in cytoplasm.
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References
Ali IKM, Ehrenkaufer GM, Hackney JA, Singh U (2007) Growth of the protozoan parasite Entamoeba histolytica in 5-azacytidine has limited effects on parasite gene expression. BMC Genomics 8(1):7. https://doi.org/10.1186/1471-2164-8-7
Ali IK, Clark CG, Petri WA (2008) Molecular epidemiology of amebiasis. Infect Genet Evol 8:698–707. https://doi.org/10.1016/j.meegid.2008.05.004
Anderson P, Kedersha N (2006) RNA granules. J Cell Biol 172(6):803–808. https://doi.org/10.1083/jcb.200512082
Bieniossek C, Papai G, Schaffitzel C, Garzoni F, Chaillet M, Scheer E, Papadopoulos P, Tora L, Schultz P, Berger I (2013) The architecture of human general transcription factor TFIID core complex. Nature 493(7434):699–702. https://doi.org/10.1038/nature11791
Bowers B, Korn ED (1968) The fine structure of Acanthamoeba castellanii. J Cell Biol 39(1):95–111. https://doi.org/10.1083/jcb.39.1.95
Brou C, Chaudhary S, Davidson I, Lutz Y, Wu J, Egly JM, Tora L, Chambon P (1993) Distinct TFIID complexes mediate the effect of different transcriptional activators. EMBO J 12(2):489–499
Bruchhaus I, Leippe M, Lioutas C, Tannich E (1993) Unusual gene organization in the protozoan parasite Entamoeba histolytica. DNA Cell Biol 12:925–933. https://doi.org/10.1089/dna.1993.12.925
Burley SK, Roeder RG (1996) Biochemistry and structural biology of transcription factor IID (TFIID). Annu Rev Biochem 65:769–799. https://doi.org/10.1146/annurev.bi.65.070196.004005
Castañón-Sánchez CA, Luna-Arias JP, de Dios-Bravo MG, Herrera-Aguirre ME, Olivares-Trejo JJ, Orozco E et al (2010) Entamoeba histolytica: a unicellular organism containing two active genes encoding for members of the TBP family. Protein Expr Purif 70(1):48–59. https://doi.org/10.1016/j.pep.2009.12.007
Chévez A, Segura M, Corona D, Iturbe-Alessio I (1972) Juxtanuclear spherules of Entamoeba histolytica. Morphological and dynamic study. Arch Invest Med (Mex) 2(Suppl 2):257–264
Cler E, Papai G, Schultz P, Davidson I (2009) Recent advances in understanding the structure and function of general transcription factor TFIID. Cell Mol Life Sci 66(13):2123–2134. https://doi.org/10.1007/s00018-009-0009-3
Curran EC, Wang H, Hinds TR, Zheng N, Wang EH (2018) Zinc knuckle of TAF1 is a DNA binding module critical for TFIID promoter occupancy. Sci Rep 8:4630. https://doi.org/10.1038/s41598-018-22879-5
Das S, Lohia A (2002) Delinking of S phase and cytokinesis in the protozoan parasite Entamoeba histolytica. Cell Microbiol 4:55–60. https://doi.org/10.1046/j.1462-5822.2002.00165.x
de Dios-Bravo G, Luna-Arias JP, Riverón AM, Olivares Trejo JJ, López Camarillo C, Orozco E (2005) Entamoeba histolytica TATA box binding protein binds to different TATA variants in vitro. FEBS J 272(6):1354–1366. https://doi.org/10.1111/j.1742-4658.2005.04566.x
Diamond LS, Harlow DR, Cunnick CC (1978) A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba. Trans R Soc Trop Med Hyg 72:431–432. https://doi.org/10.1016/0035-9203(78)90144-X
Dikstein R, Ruppert S, Tjian R (1996) TAFII250 is a bipartite protein kinase that phosphorylates the base transcription factor RAP74. Cell 84(5):781–790. https://doi.org/10.1016/S0092-8674(00)81055-7
Dynlacht BD, Hoey T, Tjian R (1991) Isolation of coactivators associated with the TATA-binding protein that mediate transcriptional activation. Cell 66(3):563–576. https://doi.org/10.1016/0092-8674(81)90019-2
Gangopadhyay SS, Ray SS, Kennady K, Pande G, Lohia A (1997) Heterogeneity of DNA content and expression of cell cycle genes in axenically growing Entamoeba histolytica HM1: IMSS clone A. Mol Biochem Parasitol 90:9–20. https://doi.org/10.1016/S0166-6851(97)00156-4
Gegonne A, Weissman JD, Singer DS (2001) TAFII55 binding to TAFII250 inhibits its acetyltransferase activity. Proc Natl Acad Sci U S A 98(22):12432–12437. https://doi.org/10.1073/pnas.211444798
Hantsche M, Cramer P (2017) Conserved RNA polymerase II initiation complex structure. Curr Opin Struct Biol 47:17–22. https://doi.org/10.1016/j.sbi.2017.03.013
Jacobson RH, Ladurner AG, King DS, Tjian R (2000) Structure and function of a human TAFII250 double bromodomain module. Science 288:1422–1425. https://doi.org/10.1126/science.288.5470.1422
Juven-Gershon T, Kadonaga JT (2010) Regulation of gene expression via the core promoter and the basal transcriptional machinery. Dev Biol 339(2):225–229. https://doi.org/10.1016/j.ydbio.2009.08.009
Kathryn L, Huisinga B, Pugh F (2004) A genome-wide housekeeping role for TFIID and a highly regulated stress-related role for SAGA in Saccharomyces cerevisiae. Mol Cell 13(4):573–585. https://doi.org/10.1016/S1097-2765(04)00087-5
Katz S, Trebicz-Geffen M, Ankri S (2014) Stress granule formation in Entamoeba histolytica: cross-talk between EhMLBP, EhRLE3 reverse transcriptase and polyubiquitinated proteins. Cell Microbiol 16(8):1211–1223. https://doi.org/10.1111/cmi.12273
Kokubo T, Gong DW, Wootton JC, Horikoshi M, Roeder RG, Nakatani Y (1994) Molecular cloning of Drosophila TFIID subunits. Nature 367(6462):484–487. https://doi.org/10.1038/367484a0
Ladurner AG1, Inouye C, Jain R, Tjian R (2003) Bromodomains mediate an acetyl-histone encoded antisilencing function at heterochromatin boundaries. Mol Cell 11:365–376. https://doi.org/10.1016/S1097-2765(03)00035-2
Lagrange T, Kapanidis AN, Tang H, Reinberg D, Ebright RH (1998) New core promoter element in RNA polymerase II-dependent transcription: sequence-specific DNA binding by transcription factor IIB. Genes Dev 12:34–44. https://doi.org/10.1101/gad.12.1.34
Lawit S, O'Grady K, Gurley W, Czarnecka Verner E (2007) Yeast two hybrid map of Arabidopsis TFIID. Plant Mol Biol 64:73–87. https://doi.org/10.1007/s11103-007-9135-1
Lee TI, Causton HC, Holstege FC, Shen WC, Hannett N, Jennings EG, Et a (2000) Redundant roles for the TFIID and SAGA complexes in global transcription. Nature 405(6787):701–704. https://doi.org/10.1038/35015104
Levecke B, Dreesen L, Dorny P, Verweij JJ, Vercammen F, Casaert S, Vercruysse J, Geldhof P (2010) Molecular identification of Entamoeba spp. in captive nonhuman primates. J Clin Microbiol 48(8):2988–2990. https://doi.org/10.1128/JCM.00013-10
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)). Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Loftus B, Anderson I, Davies R, Alsmark UCM, Samuelson J, Amedeo P, Roncaglia P, Berriman M, Hirt RP, Mann BJ, Nozaki T, Suh B, Pop M, Duchene M, Ackers J, Tannich E, Leippe M, Hofer M, Bruchhaus I, Willhoeft U, Bhattacharya A, Chillingworth T, Churcher C, Hance Z, Harris B, Harris D, Jagels K, Moule S, Mungall K, Ormond D, Squares R, Whitehead S, Quail MA, Rabbinowitsch E, Norbertczak H, Price C, Wang Z, Guillén N, Gilchrist C, Stroup SE, Bhattacharya S, Lohia A, Foster PG, Sicheritz-Ponten T, Weber C, Singh U, Mukherjee C, el-Sayed NM, Petri WA, Clark CG, Embley TM, Barrell B, Fraser CM, Hall N (2005) The genome of the protist parasite Entamoeba histolytica. Nature 433:865–868. https://doi.org/10.1038/nature03291
Loomis MR, Britt JO Jr, Gendron AP, Holshuh HJ, Howard EB (1983) Hepatic and gastric amebiasis in black and white colobus monkeys. J Am Vet Med Assoc 183(11):1188–1191
López-Casamichana M, Orozco E, Marchat LA, López-Camarillo C (2008) Transcriptional profile of the homologous recombination machinery and characterization of the EhRAD51 recombinase in response to DNA damage in Entamoeba histolytica. BMC Mol Biol 9:35. https://doi.org/10.1186/1471-2199-9-35
Lorenzi HA, Puiu D, Miller JR, Brinkac LM, Amedeo P, Hall N, Caler EV (2010) New assembly, reannotation and analysis of the Entamoeba histolytica genome reveal new genomic features and protein content information. PLoS Negl Trop Dis 4:e716. https://doi.org/10.1371/journal.pntd.0000716
Luna-Arias JP, Hernandez-Rivas R, de Dios-Bravo G, Garcia J, Mendoza L, Orozco E (1999) The TATA-box binding protein of Entamoeba histolytica: cloning of the gene and location of the protein by immunofluorescence and confocal microscopy. Microbiol 145(1):33–40. https://doi.org/10.1099/13500872-145-1-33
Manna D, Ehrenkaufer GM, Singh U (2014) Regulation of gene expression in the protozoan parasite Entamoeba invadens: identification of core promoter elements and promoters with stage-specific expression patterns. Int J Parasitol 44(11):837–845. https://doi.org/10.1016/j.ijpara.2014.06.008
Martinez E, Kundu TK, Fu J, Roeder RG (1998) A human SPT3-TAFII31-GCN5-L acetylase complex distinct from transcription factor IID. J Biol Chem 273:23781–23785. https://doi.org/10.1074/jbc.273.37.23781
Matangkasombut O, Buratowski S (2003) Different sensitivities of bromodomain factors 1 and 2 to histone H4 acetylation. Mol Cell 11(2):353–363. https://doi.org/10.1016/S1097-2765(03)00033-9
Matangkasombut O, Buratowski RM, Swilling NW, Buratowski S (2000) Bromodomain factor 1 corresponds to a missing piece of yeast TFIID. Genes Dev 14(8):951–962. https://doi.org/10.1101/gad.14.8.951
Mizzen CA, Yang XJ, Kokubo T, Brownell JE, Bannister AJ, Owen-Hughes T et al (1996) The TAF (II) 250 subunit of TFIID has histone acetyltransferase activity. Cell 87(7):1261–1270. https://doi.org/10.1016/S0092-8674(00)81821-8
Moqtaderi Z, Yale JD, Struhl K, Buratowski S (1996) Yeast homologues of higher eukaryotic TFIID subunits. Proc Natl Acad Sci U S A 93(25):14654–14658. https://doi.org/10.1073/pnas.93.25.14654
Nagy Z, Tora L (2007) Distinct GCN5/PCAF-containing complexes function as co-activators and are involved in transcription factor and global histone acetylation. Oncogene 26:5341–5357. https://doi.org/10.1038/sj.onc.1210604
Narayanasamy RK, Castañón-Sanchez CA, Luna-Arias JP, García-Rivera G, Avendaño-Borromeo B, Labra-Barrios ML, Valdés J, Herrera-Aguirre ME, Orozco E (2018) The Entamoeba histolytica TBP and TRF1 transcription factors are GAAC-box binding proteins, which display differential gene expression under different stress stimuli and during the interaction with mammalian cells. Parasit Vectors 11(1):153. https://doi.org/10.1186/s13071-018-2698-7
Ogryzko VV, Kotani T, Zhang X, Schiltz RL, Howard T, Yang XJ, Howard BH, Qin J, Nakatani Y (1998) Histone-like TAFs within the PCAF histone acetylase complex. Cell 94:35–44. https://doi.org/10.1016/S0092-8674(00)81219-2
Orozco E, Guarneros G, Martinez-Palomo A, Sánchez T (1983) Entamoeba histolytica. Phagocytosis as a virulence factor. J Exp Med 158(5):1511–1521. https://doi.org/10.1084/jem.158.5.1511
Papai G, Tripathi MK, Ruhlmann C, Werten S, Crucifix C, Weil PA, Schultz P (2009) Mapping the initiator binding Taf2 subunit in the structure of hydrated yeast TFIID. Structure 17(3):363–373. https://doi.org/10.1016/j.str.2009.01.006
Poon D, Weil PA (1993) Immunopurification of yeast TATA-binding protein and associated factors. J Biol Chem 268(21):15325–15328
Purdy JE, Lana TP, Mann BJ, Petri WA (1996) Upstream regulatory elements controlling expression of the Entamoeba histolytica lectin. Mol Biochem Parasitol 78:91–103. https://doi.org/10.1016/S0166-6851(96)02614-X
Ralston KS, Solga MD, Mackey-Lawrence NM, Somlata BA, Petri WA (2014) Trogocytosis by Entamoeba histolytica contributes to cell killing and tissue invasion. Nature 508:526–530. https://doi.org/10.1038/nature13242
Ravdin JI, Guerrant RL (1981) Role of adherence in cytopathogenic mechanisms of Entamoeba histolytica. Study with mammalian tissue culture cells and human erythrocytes. J Clin Invest 68:1305–1313. https://doi.org/10.1172/JCI110377
Reese JC, Apone L, Walker SS, Griffin LA, Green MR (1994) Yeast TAFIIS in a multisubunit complex required for activated transcription. Nature 371(6497):523–527. https://doi.org/10.1038/371523a0
Ruppert S, Tjian R (1995) Human TAFII250 interacts with RAP74: implications for RNA polymerase II initiation. Genes Dev 9:2747–2755. https://doi.org/10.1101/gad.9.22.2747
Ruppert S, Wang Edith H, Tjian R (1993) Cloning and expression of human TAFII250: a TBP-associated factor implicated in cell-cycle regulation. Nature 362:175–179. https://doi.org/10.1038/362175a0
Sekiguchi T, Miyata T, Nishimoto T (1988) Molecular cloning of the cDNA of human X chromosomal gene (CCG1) which complements the temperature-sensitive G1 mutants, tsBN462 and ts13, of the BHK cell line. EMBO J 1988(6):1683–1687
Sekiguchi T, Nohiro Y, Nakamura Y, Hisamoto N, Nishimoto T (1991) The human CCG1 gene, essential for progression of the G1 phase, encodes a 210-kilodalton nuclear DNA-binding protein. Mol Cell Biol 11(6):3317–3325. https://doi.org/10.1128/MCB.11.6.3317
Shrimal S, Bhattacharya S, Bhattacharya A (2010) Serum-dependent selective expression of EhTMKB1-9, a member of Entamoeba histolytica B1 family of transmembrane kinases. PLoS Pathog 6(6):e1000929. https://doi.org/10.1371/journal.ppat.1000929
Singh U, Rogers JB, Mann BJ, Petri WA (1997) Transcription initiation is controlled by three core promoter elements in the hgl5 gene of the protozoan parasite Entamoeba histolytica. Proc Natl Acad Sci U S A 94:8812–8817. https://doi.org/10.1073/pnas.94.16.8812
Singh U, Gilchrist CA, Schaenman JM, Rogers JB, Hockensmith JW, Mann BJ et al (2002) Context-dependent roles of the Entamoeba histolytica core promoter element GAAC in transcriptional activation and protein complex assembly. Mol Biochem Parasitol 120(1):107–116. https://doi.org/10.1016/S0166-6851(01)00441-8
Steinbuch M, Audran R (1969) The isolation of IgG from mammalian sera with the aid of caprylic acid. Arch Biochem Biophys 134(2):279–284. https://doi.org/10.1016/0003-9861(69)90285-9
Tachibana H, Yanagi T, Lama C, Pandey K, Feng M, Kobayashi S, Sherchand JB (2013) Prevalence of Entamoeba nuttalli infection in wild rhesus macaques in Nepal and characterization of the parasite isolates. Parasitol Int 62(2):230–235. https://doi.org/10.1016/j.parint.2013.01.004
Trowitzsch S, Viola C, Scheer E, Conic S, Chavant V, Fournier M et al (2015) Cytoplasmic TAF2-TAF8-TAF10 complex provides evidence for nuclear holo-TFIID assembly from preformed submodules. Nat Commun 14(6):6011. https://doi.org/10.1038/ncomms7011
Wang H, Curran EC, Hinds TR, Wang EH, Zheng N (2014) Crystal structure of a TAF1-TAF7 complex in human transcription factor IID reveals a promoter binding module. Cell Res 24(12):1433–1444. https://doi.org/10.1038/cr.2014.148
Weber C, Guigon G, Bouchier C, Frangeul L, Moreira S, Sismeiro O, Gouyette C, Mirelman D, Coppee JY, Guillén N (2006) Stress by heat shock induces massive down regulation of genes and allows differential allelic expression of the Gal/GalNAc lectin in Entamoeba histolytica. Eukaryot Cell 5:871–875. https://doi.org/10.1128/EC.5.5.871-875.2006
Weber C, Marchat LA, Guillén N, Lopez-Camarillo C (2009) Effects of DNA damage induced by UV irradiation on gene expression in the protozoan parasite Entamoeba histolytica. Mol Biochem Parasitol 164:165–169. https://doi.org/10.1016/j.molbiopara.2008.12.005
Weedall GD, Hall N (2011) Evolutionary genomics of Entamoeba. Res Microbiol 162(6):637–645. https://doi.org/10.1016/j.resmic.2011.01.007
Wieczorek E, Brand M, Jacq X, Tora L (1998) Function of TAF (II)-containing complex without TBP in transcription by RNA polymerase II. Nature 393:187–191. https://doi.org/10.1038/30283
Wright KJ, Marr MT 2nd, Tjian R (2006) TAF4 nucleates a core subcomplex of TFIID and mediates activated transcription from a TATA-less promoter. Proc Natl Acad Sci U S A 103(33):12347–12352. https://doi.org/10.1073/pnas.0605499103
Acknowledgments
The authors are grateful to Dr. Javier Cázares-Apátiga for his technical support in confocal microscopy experiments, Emmanuel Ríos-Castro MSc. for his technical support in MS analysis at the Unidad de Genómica, Proteómica y Metabolómica (UGPM), LaNSE, Cinvestav-IPN, and Cesar Isaac Bazán-Méndez for spelling and grammar review of manuscript.
Funding
We are grateful to the National Council of Science and Technology of Mexico (CONACyT) for the support to this work with the Grant number CB-2009-132020-B to Dr. Juan Pedro Luna-Arias, and for the PhD fellowship to Bartolo Avendaño Borromeo (CVU 229747).
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BA-B, performed, designed the experiments, discussed the results, and wrote the manuscript; RKN, designed the experiments; GG-R, helped in some experiments with E. histolytica trophozoites, MLL-B, participated in the generation of antibodies and Western blots; AEL-G, performed the electron microscopy experiments; BCHM, designed and performed the electron microscopy experiments; CAC-S, discussed experiments and results; EO, supplied the E. histolytica strain and laboratory facilities for the development of some experiments; JPL-A, conducted experiments, discussed experiments and results, wrote and revised the manuscript.
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Avendaño-Borromeo, B., Narayanasamy, R.K., García-Rivera, G. et al. Identification of the gene encoding the TATA box-binding protein-associated factor 1 (TAF1) and its putative role in the heat shock response in the protozoan parasite Entamoeba histolytica. Parasitol Res 118, 517–538 (2019). https://doi.org/10.1007/s00436-018-6170-6
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DOI: https://doi.org/10.1007/s00436-018-6170-6